Folia Morphol.

Vol. 77, No. 4, pp. 656–669

DOI: 10.5603/FM.a2018.0016
ORIGINAL ARTICLE Copyright © 2018 Via Medica
ISSN 0015–5659
www.fm.viamedica.pl

Anatomy of the feeding arteries of the

cerebral arteriovenous malformations
B. Milatović1, J. Saponjski2, H. Huseinagić3, M. Moranjkić4, S. Milošević Medenica5,
I. Marinković6, I. Nikolić7, S. Marinkovic8
1
Centre for Radiology, Clinic of Neurosurgery, Clinical Centre of Serbia, Belgrade, Serbia
2
Clinic of Cardiovascular Surgery, Clinical Centre of Serbia, Belgrade, Serbia
3
Department of Radiology, Faculty of Medicine, Kallos University, Tuzla, Bosnia and Herzegovina
4
Department of Neurosurgery, Faculty of Medicine, Kallos University, Tuzla, Bosnia and Herzegovina
5
Centre for Radiology, Clinical Centre of Serbia, Belgrade, Serbia
6
Department of Neurology, Helsinki University Central Hospital, Finland
7
Clinic for Neurosurgery, Clinical Centre of Serbia, Belgrade, Serbia
8
Institute of Anatomy, Faculty of Medicine, University of Belgrade, Belgrade, Serbia

[Received: 8 January 2018; Accepted: 30 January 2018]

Background: Identification and anatomic features of the feeding arteries of the

arteriovenous malformations (AVMs) is very important due to neurologic, radio-
logic, and surgical reasons.
Materials and methods: Seventy-seven patients with AVMs were examined by
using a digital subtraction angiographic (DSA) and computerised tomographic (CT)
examination, including three-dimensional reconstruction of the brain vessels. In
addition, the arteries of 4 human brain stems and 8 cerebral hemispheres were
microdissected.
Results: The anatomic examination showed a sporadic hypoplasia, hyperplasia,
early bifurcation and duplication of certain cerebral arteries. The perforating
arteries varied from 1 to 8 in number. The features of the leptomeningeal and
choroidal vessels were presented. The radiologic examination revealed singular
(22.08%), double (32.48%) or multiple primary feeding arteries (45.45%), which
were dilated and elongated in 58.44% of the patients. The feeders most often
originated from the middle cerebral artery (MCA; (23.38%), less frequently from
the anterior cerebral artery (ACA; 12.99%), and the posterior cerebral artery
(PCA; 10.39%). Multiple feeders commonly originated from the ACA and MCA
(11.69%), the MCA and PCA (10.39%), the ACA and PCA (7.79%), and the ACA,
MCA and PCA (5.19%). The infratentorial feeders were found in 9.1% of the
AVMs. Contribution from the middle meningeal and occipital arteries was seen
in 3.9% angiograms. Two cerebral arteries had a saccular aneurysm. The AVM
haemorrhage appeared in 63.6% of patients.
Conclusions: The knowledge of the origin and anatomic features of the AVMs
feeders is important in the explanation of neurologic signs, and in a decision
regarding the endovascular embolisation, neurosurgical and radiosurgical treat-
ments. (Folia Morphol 2018; 77, 4: 656–669)

Key words: angiography, arteriovenous malformations, cerebral arteries,

feeding arteries, neuroanatomy, neuroradiology, neurosurgery

Address for correspondence: S. Marinković, MD, PhD, Professor of Neuroanatomy, Institute of Anatomy, Faculty of Medicine, Dr. Subotić 4/2,
11000 Belgrade, Serbia, e-mail: mocamarinkovic@med.bg.ac.rs

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 B. Milatović et al., Feeding arteries of the AVMs
INTRODUCTION
Each cerebral arteriovenous malformation (AVM)
represents an abnormal vascular network (the nidus)
of dilated and tortuous arteries and veins without
a capillary bed among them or with some micro-
vasculature in its nidus [16, 29, 47, 68, 78, 80].
The AVMs receive one or more feeding arteries, and
contain the intranidal network, as well as one or
several draining veins.
The feeding vessels may originate from the in-
ternal carotid artery (ICA), and some additional ves-
sels occasionally from the external carotid artery
(ECA). More often, however, they arise from the
anterior (ACA), middle (MCA) or posterior cerebral
artery (PCA), and in some cases from the posterior
communicating artery (PComA), anterior choroidal
artery (AChA), or the medial (MPChA) or lateral
posterior choroidal arteries (LPChA), as well as from
the basilar (BA) or vertebral arteries (VA), that is,
from their corresponding branches: the superior
cerebellar (SCA), anterior inferior cerebellar (AICA),
and posterior inferior cerebellar arteries (PICA), as
well as from the small medullary and pontine twigs
[16, 18, 24, 26, 78]. One or more of the mentioned
vessels may supply a single AVM, either from the
same or different sources.
A precise identification of the feeding vessels was
performed only sporadically by neuroradiologists and
neurosurgeons [16, 18, 24, 27, 46, 78]. In general,
the parent arteries were determined, and rarely their
branches which directly supplied certain AVMs. In
fact, there are no articles in the available literature
dealing systematically with the feeding arteries. Yet,
the anatomic knowledge of the feeders is clinically
very important for several reasons. Firstly, the involve-
ment of certain feeders and location of their AVMs
can usually explain neurologic signs and symptoms
in patients. Secondly, feeders are used during the
endovascular interventional radiologic procedure
[16, 50–53, 80]. Thirdly, some feeders are the site of
neurosurgical intervention [14, 18, 24, 27, 45, 69, 78].
Finally, they can be the site of arterial aneurysms
[1, 10, 16, 19, 54, 56].
Accordingly, the aim of our study was, firstly, to
identify each single feeding vessel of the AVMs and
its parent artery in our patients. Secondly, to deter-
mine the anatomic features of the feeders, and their
relationship with a local AVM and the brain region
involved. And thirdly, to consider the therapeutic
implications of the obtained anatomic facts.
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MATERIALS AND METHODS
Fifty-seven patients from the Clinic of Neurosur-
gery of the University of Belgrade were included in this
study, as well as an additional 20 patients from the
Department of Radiology of the University of Tuzla.
The material regarding these 77 patients was collect-
ed in the period from January 2016 to February 2017.
Each patient had a personal history, as well as
serial computerised tomographic (CT) and digital
subtraction angiographic (DSA) images, while 18 of
them had an additional neurosurgical report. Most
of the DSA and CT imaging techniques, including
neurosurgical operations, were performed by the
authors of this study.
The CT examination was done in a Siemens So-
matom Definition AS 128-slice scanner (rotation time
0.5 s, pitch 0.5, slice thickness 0.6 mm, 120–140 kV
interval, manual 260 mA, noise index 3). A CT cerebral
angiography (CTA) was performed as well, using Ul-
travist 370 as a contrast medium (bolus 100 mL, flow
of contrast 4 mL/s). Multiplanar reconstruction and
volume rendering were made of the skull and blood
vessels to get three-dimensional (3D) CTA images.
The DSA in all patients was performed by the
Seldinger’s method, i.e. by a transfemoral cathe-
terisation followed by an automatic injection of the
contrast substance (Omnipaque) in a bolus of 5–8 mL
per each sequence, in order to obtain a four vessel
cerebral angiography. In addition, a 3D vascular re-
construction was made in several patients. This was
done by using a monoplane DSA unit with rotational
capabilities (Siemens Healthcare, Axiom Artis). Typ-
ically, 6–10 mL of Ultravist 370 was applied, when
one anteroposterior, one lateral, and one or two
oblique angiograms were made of the carotid and
vertebrobasilar systems. The field of view was 38-cm2
for the anteroposterior images, and 30-cm2 for the
lateral and oblique images, whilst a 1024 × 1024
matrix was used. The spatial resolution was 0.32
× 0.32 mm. The 3D DSA typically involved a 1–3 sec-
ond delay, followed by a 2.5 mL/s injection of a total
12–15 mL. The images were reconstructed in a 256
× 256 matrix. The rotational angiographic data were
transferred to an independent workstation (Siemens
Healthcare, Leonardo Workplace) for the generation
of 3D reformatted images.
The obtained images of each patient were ana-
lysed by one group, and then independently by anoth-
er group of the authors, in order to identify the parent
and feeding arteries. The appearance of each feeder
 Folia Morphol., 2018, Vol. 77, No. 4

Figure 1. The leptomeningeal (pial) branches of the main cerebral arteries. A. Branches of the anterior and posterior cerebral arteries on the
medial and inferior surface of the cerebral hemisphere. 1 — the A2 segment. Note the medial orbitofrontal artery (2), frontopolar (3), perical-
losal (4), callosomarginal (5), the anterior (6), middle (7) and posterior internal frontal (8), paracentral (9), superior parietal (10), and the pre-
cuneal arteries (11). Also note the P2 segment of the posterior cerebral artery (12), the parieto-occipital (13), calcarine (14), and the posterior
temporal (15), middle temporal (16) and anterior temporal arteries (17). B. The leptomeningeal branches of the middle cerebral artery on the
superolateral surface of the hemisphere. Note the prefrontal arteries (1), precentral (2), central (3), anterior parietal (4), posterior parietal (5),
angular gyrus (6), temporo-occipital (7), and the posterior temporal (8), middle temporal (9) and anterior temporal arteries (10).

was then examined carefully. The mentioned imaging
procedures were approved by the authorities of the
Clinic of Neurosurgery, Department of Radiology, and
the Ethics Committee of the University Clinical Centre.
Statistically, the frequencies of the feeders and their
parent arteries were counted.
Finally, the arteries of 4 brain stems and 8 cerebral
hemispheres, taken from routine autopsies, were
washed out with a 10% saline solution and perfused
with a 10% mixture of India ink and gelatine. The
specimens were then immersed in a 10% formalde-
hyde solution for 3 weeks. Thereafter, the arteries
were carefully dissected under a stereo-microscope
(Leica MZ6) using neurosurgical microinstruments.
Drawings of the vessels were made in each speci-
men, and two common drawings were designed to
illustrate the arteries in this study.
RESULTS
We examined first the arteries in the anatomic
specimens, and then those in the carotid and vertebral
angiograms of our patients with the AVMs.
Anatomic specimens
The dissection of 4 brain stems and 8 cerebral
hemispheres facilitated an anatomic examination of
the trunks and branches of the ICA, ACA, MCA, AChA,
the anterior communicating artery (AComA), the
PComA, the PCA, and also the VA and BA, including
their cerebellar branches (the PICA, AICA, and SCA),
as well as the medullary and pontine twigs.
As regards the supraclinoid (C4) segment of the
ICA, it always gave rise to the typical side and the ter-
minal branches, i.e. the PComA, AChA, ACA and MCA,
but also occasionally to the uncal branch (12.5%), and
1–4 perforating twigs in all the cases.
The ACA had, more or less, a typical appearance
in the examined specimens. In only 1 case a hypo-
plasia of its proximal (A1) segment was observed.
This segment gave off 1–3 perforating twigs, as well
as the recurrent artery of Heubner in 12.5% of the
specimens. The distal (A2) segment usually divided
into the pericallosal and the callosomarginal artery
close to the genu of the corpus callosum. It gave rise
to Heubner’s artery in 25% of the cases. All the lep-
tomeningeal branches originated from this segment
and from the mentioned two terminal stems (Fig. 1A).
As regards the anterior communicating artery
(AComA), which interconnects the right and left ACA,
it always gave off 1–4 hypothalamic twigs in front of
the lamina terminalis, and a large subcallosal artery. As
for Heubner’s artery of the ACA, it was seen in 62.5%
of the specimens to originate at the AComA level.
The MCA showed a typical proximal (M1) segment
in all specimens but one, in which an early bifurcation
was noticed. It gave rise to 2–8 perforating (lenticu-
lostriate) twigs, as well as to the lateral orbitofrontal,
uncal, temporopolar, and anterior temporal arteries
in most of the cases. The insular (M2) segment was
singular in 1 case, duplicated in 6, and triplicated in
1 specimen. This segment, along with its insulo-oper-
cular stems, gave off all the superficial leptomeningeal

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 B. Milatović et al., Feeding arteries of the AVMs
branches which spread radially from the Sylvian fissure
across the superolateral surface of the cerebral hem-
ispheres without major anatomic variants (Fig. 1B).
The AChA, which arose between the PComA ori-
gin site and the ICA bifurcation point, coursed close
to the optic tract and the anteromedial part of the
temporal lobe, and then entered the choroid plexus
of the temporal horn of the lateral ventricle. It gave
rise to 1 to 5 perforating arteries, an uncal branch,
the optic, peduncular and geniculate twigs, and
a few larger choroidal vessels.
The PComA was a small branch of the ICA in
7 specimens, whilst in one case it was a large vessel
which continued posteriorly as the distal segment of
the PCA (the so-called foetal PCA origin). The PComA
gave rise to several hypothalamic, optic, peduncu-
lar, and mammillary twigs, and to one perforating
branch, i.e. the premammillary (tuberothalamic or
anterior thalamoperforating) artery.
The PCA had a typical proximal (P1) segment, ex-
cept in 1 case where the latter segment showed a mild
hypoplasia. It occasionally gave rise to the peduncular
and mammillary branches, to 1–4 thalamoperforating
(TPA) and the mesencephalic perforating twigs, as well
as to a single collicular artery in 7 cases. As regards the
TPA themselves, they varied from 0 to 3 in number. In
the former case, such an artery was absent on one side,
but the opposite TPA was very large and suppled the
portions of both the right and left thalamus.
The ambient (P2) segment gave off the peduncular
and tegmental twigs in all the specimens, the colli-
cular artery in 1 case, from 2 to 6 thalamogeniculate
perforators, the medial and lateral posterior choroidal
arteries, the splenial branch, the uncal, hippocam-
pal and parahippocampal vessels, and commonly
the anterior temporal artery. The quadrigeminal (P3)
segment usually gave rise to the middle and pos-
terior temporal arteries, and then divided into the
parieto-occipital and calcarine arteries (Fig. 1A). The
mentioned MPChA varied from 1 to 3 in number, but
most often two were present, i.e. a proximal and
a distal one. The LPChA ranged from 1 to 5 in number,
but usually only two of them were larger in size.
The terminal (medullary) segment of the VA was
typical in 7 cases and hypoplastic on the left side in
one specimen. It gave rise to the perforating twigs, the
anterolateral and lateral medullary branches, the root
of the anterior spinal artery, and the PICA. Similarly,
the BA gave off the right and left perforating, antero-
lateral and lateral pontine vessels, as well as the cere-
659
bellar arteries, i.e. the AICA and SCA, in all specimens.
A unilateral duplication of the SCA was seen in 1 case,
and an early bifurcation in another specimen.
The cerebral arteries were noticed to give off
three types of the side and terminal branches: the
leptomeningeal, the perforating, and the choroidal.
The leptomeningeal (pial) arteries nourished the pe-
ripheral part of the cerebrum, cerebellum and brain
stem (Figs. 1A, B). The perforating vessels supplied
the central or the paramedian part of the mentioned
neural portions, and most of the thalamus. The cho-
roidal branches mainly perfused the choroid plexus
and the walls of the ventricles.
Angiographic specimens
We examined the feeding arteries and parent
vessels, but also the AVMs location and the draining
veins, in several hundreds of DSA, CT, and CTA images.
The radiologic appearance of the feeding arteries was
described, and the identification of each single feeder
and its parent vessel was made of all the mentioned
intracranial arteries, and occasionally of certain ex-
tracranial vessels.
Origin and number of the feeding arteries
Some of the examined AVMs had a single supply-
ing vessel, while the remaining received two or several
feeding arteries, either from the same or different
parent arteries, whose normal anatomic position,
course and branching pattern were presented in the
mentioned Figures 1A, B.
A single primary feeder was noticed in 22.08% of
the AVMs. It most often belonged to the ACA (Fig. 2),
less frequently to the MCA (Fig. 3) and the PCA, and
rarely to the ICA or the cerebellar branches of the BA
(Fig. 4). All the singular feeders were the leptomenin-
geal (pial) vessels, except in two patients in whom
they comprised a perforating MCA twig (Fig. 3).
Two primary feeders were found in 32.48% of
the AVMs (Figs. 5–7). They can take origin from the
same or different parent arteries. Certain feeders
arose from the ACA, some others from the MCA
(Figs. 5, 6) or the PCA (Fig. 7), or from the infratentorial
arteries. The majority of the feeders belonged to the
leptomeningeal branches, but some of them to the
perforating or the choroidal arteries as well.
Finally, 3–6 primary feeders were seen in the re-
maining 45.45% of the AVMs. They usually originat-
ed from different parent arteries, e.g. two feeders
from the ACA, and one from the MCA and the PCA,
 Folia Morphol., 2018, Vol. 77, No. 4
Figure 2. One source and one primary feeder of an arteriovenous
malformation (asterisks) on the ventromedial surface of the su-
perior frontal gyrus, which is fed by branches of the frontopolar
artery (1). Note an aneurysm (2) of the latter artery at its branching
site, as well as a draining vein (3). 4 — the internal carotid artery;
5 — the A2 segment of the right anterior cerebral artery; 6 — the
pericallosal artery. Lateral and slightly oblique carotid three-dimen-
sional angiogram.
Figure 3. A small arteriovenous malformation (asterisk) in the head
of the caudate nucleus is supplied by a lenticulostriate branch (1)
of the M1 segment (2) of the left middle cerebral artery. Note
a postnidal vein (3), which drains into the sphenoparietal sinus,
and the A2 segment (4) of the left anterior cerebral artery. The
anteroposterior carotid angiogram.
respectively, within the supratentorial compartment
(Fig. 8). Several feeders can be observed in the in-
fratentorial compartment as well, e.g. the SCA, AICA
and PICA (Fig. 9). Multiple feeders belonged to the
660
Figure 4. One source within the infratentorial compartment, i.e. in
the posterior cranial fossa. An arteriovenous malformation (asterisks),
which is mainly located on the superolateral part of the pons, is fed
by a large left superior cerebellar artery (1). 2 — the left posterior
cerebral artery; 3 — the basilar artery; 4 and 5 — the left and right
anterior inferior cerebellar arteries; 6 — the right superior cerebel-
lar artery; 7 — the right posterior cerebral artery. The anteroposte-
rior vertebral angiogram.
Figure 5. Two feeding vessels from the middle cerebral artery.
A lateral and slightly oblique view of an arteriovenous malformation
(asterisk) in the fronto-opercular region, which is supplied by two
prefrontal arteries arising from the superior (or anterior) terminal
trunk (1) of the left middle cerebral artery. 2 — the precentral
arteries; 3 — the central artery; 4 — the inferior terminal trunk;
5 — the A2 segment of the anterior cerebral artery.
leptomeningeal vessels, but some of them were of
the perforating or the choroidal type (Fig. 10).
Regardless of their number (except in the case
with a singular vessel), the feeders may arise, as
already mentioned, from the same parent artery or
from different arteries (Table 1). In the former cases,
 B. Milatović et al., Feeding arteries of the AVMs
Figure 6. Another two feeding vessels from the middle cerebral ar-
tery. An arteriovenous malformation (AVM) (asterisks) is mainly lo-
cated on the posterior part of the left superior temporal and middle
temporal gyri. Its feeding vessels comprise the angular gyrus artery
(1) and the temporo-occipital artery (2). Note the superior parietal
branch (3) of the middle cerebral artery, and the pericallosal (4) and
callosomarginal artery (5) of the anterior cerebral artery. The AVM
contains several small intranidal aneurysms. The lateral carotid
angiogram.
Figure 7. A corticosubcortical anterior cerebral artery (AVM)
(asterisk) which is mainly located in the posterior part of the lateral
and medial occipitotemporal gyri. This AVM is predominantly fed
by a large posterior temporal branch (1) of the posterior cerebral
artery, and only slightly by the calcarine artery (2). Note the parieto-
-occipital artery (3), the lateral and medial posterior choroidal arter-
ies (4), the mesencephalic perforators (5), the thalamoperforating
arteries (6), and the left posterior cerebral artery (7). The lateral
vertebral angiogram.
the feeders most often originated from the MCA
(23.38%), less frequently from the ACA (12.99%)
and the PCA (10.39%), and rarely from the ICA or
661
Figure 8. Three sources and four primary feeders of an anterior
cerebral artery (asterisk) within the supratentorial compartment,
i.e. in the parieto-occipital region. Note the callosomarginal (1)
and the pericallosal artery (2) of the anterior cerebral artery, the
posterior parietal artery (3) of the middle cerebral artery, and the
parieto-occipital artery (4) of the posterior cerebral artery, the latter
presenting a carotid origin. The lateral carotid angiogram.
Figure 9. Three feeders in the infratentorial compartment. An ante-
rior cerebral artery (asterisk) receives blood from the left superior
cerebellar artery (1), the anterior inferior cerebellar artery (2), and
the posterior inferior cerebellar artery (3). Note the vertebral artery
(4), the basilar artery (5), and the left posterior cerebral artery (6).
The lateral vertebral three-dimensional angiogram.
the cerebellar arteries (Table 1). The feeders of some
AVMs arose from two different parent arteries, most
often from the ACA and MCA (11.69%), as well as
from the MCA and PCA (10.39%), and ACA and PCA
(7.79%) (Table 1). In 1 patient the AVM was supplied
by both ACAs, i.e. by the pericallosal and calloso-
 Folia Morphol., 2018, Vol. 77, No. 4

Table 1. Origin of the feeding vessels

Parent arteries Frequency
ICA 1.30%
ACA 12.99%
MCA 23.38%
PCA 10.39%
SCA 2.60%
AICA 1.30%
ACA–ACA 1.30%
ACA–MCA 11.69%
Figure 10. Four feeders from the same parent artery (posterior ACA–PCA 7.79%
cerebral artery), and one from the posterior communicating artery. MCA–PCA 10.39%
A large anterior cerebral artery (AVM) (asterisk) occupies the
anterior part and the adjacent superolateral portion of the thalamus. AChA–PCA 1.30%
The AVM is supplied by the premammillary perforator (1) from the PComA–PCA 1.30%
posterior communicating artery (2), and by the thalamogeniculate
SCA–AICA 3.89%
branch (3), the medial posterior choroidal artery (4), and two lateral
posterior choroidal arteries (5) from the posterior cerebral artery (6). ACA–MCA–PCA 5.19%
Note the superior cerebellar artery (7). The lateral and slightly SCA–AICA–PICA 1.30%
oblique vertebral angiogram.
MCA–PCA–ECA 2.60%
ACA–MCA–PCA–ECA 1.30%
marginal arteries on the ipsilateral side, and by the
ACA — anterior cerebral artery; AChA — anterior choroidal artery; AICA — anterior
callosomarginal artery on the opposite side. Finally, inferior cerebellar artery; ICA — internal carotid artery; ECA — external carotid artery;
MCA — middle cerebral artery; LPChA lateral posterior choroidal arteries; MPChA —
multiple feeders were noticed to originate from three
medial posterior choroidal arteries; PCA — posterior cerebral artery; PComA — poste-
or four parent arteries, most often from the ACA, rior communicating artery; PICA — posterior inferior cerebellar artery; SCA — superior
cerebellar artery
MCA and PCA (Fig. 8, Table 1). In 3 of these patients,
there was also a contribution of the ECA (Table 1),
i.e. of the middle meningeal and occipital arteries.
Table 2. Feeding arteries of the supratentorial arteriovenous
The primary feeders (Table 2) were identified as the
malformations (AVMs)
following: the primitive trigeminal artery of the ICA; the
Source Type of arteries
pericallosal, callosomarginal, frontopolar, and posteri-
or internal frontal branches of the ACA; the prefrontal, ICA Primitive trigeminal
central, anterior and posterior parietal, angular gyrus, ACA Pericallosal
Callosomarginal
temporo-occipital, and perforating (lenticulostriate)
Frontopolar
branches of the MCA; the choroidal twigs of the AChA; Posterior internal frontal
the premammillary branch of the PComA; the parie- MCA Prefrontal
to-occipital, calcarine, collicular, posterior temporal, Central
and the perforating branches of the PCA, including Anterior parietal
Posterior parietal
the choroidal vessels (the MPChA and LPChA); and,
Angular gyrus
the small twigs of the SCA, AICA and PICA. Most of Temporo-occipital
the feeders belonged to the leptomeningeal branches, Lenticulostriate
and others to the perforating or the choroidal vessels. AChA Choroidal
There were also certain combinations of these types PComA Premammillary
of the feeders of some AVMs (Fig. 10).
PCA Parieto-occipital
Calcarine
The appearance of feeding arteries Posterior temporal
Collicular
The feeders in the majority of the AVMs (58.44%) Thalamoperforating
were dilated and elongated, often showing a tortuous Thalamogeniculate
course (Figs. 5–8). Although the vessel diameters were Medial posterior choroidal
Lateral posterior choroidal
not measured directly, it was obvious that the lumen
of some of them was much larger than that of the Abbreviations — see Table 1

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 B. Milatović et al., Feeding arteries of the AVMs
similar adjacent arteries, or of the same vessels of the
opposite hemisphere. The enlargement and tortuos-
ity were especially expressed in the cases of multiple
leptomeningeal feeders, arising either from a single or
several parent arteries, and in large-sized AVMs (Fig. 8).
Finally, in 2 patients we observed an aneurysm on
the feeding arteries. One was located at the branching
site of a feeder (Fig. 2), and another one on the supracli-
noid segment of the ICA. In addition, intranidal (Fig. 6)
and postnidal venous pouches or aneurysms were
noticed in 9 patients. Some of them were more than
3 cm in diameter. Aneurysms are one of the causes
of an intracranial haemorrhage, which was observed
in 63.6% of the AVMs in our patients.
DISCUSSION
We shall first shortly consider the vascular ana-
tomic data, and then the AVMs pathogenesis, the
anatomic features of the feeding arteries and their
parent vessels, and finally their clinical significance.
Anatomic aspect
Dissected specimens in our study helped to identify
each feeding artery in the carotid and vertebral angio-
grams of our patients, i.e. the corresponding leptome-
ningeal, perforating and choroidal branches. All the
identified vessels were checked in the corresponding
publications [6, 7, 12, 15–17, 20, 22, 25, 37, 38, 57,
64, 66, 67, 72, 76]. The results of our anatomic study
were in accordance with data in the latter reports.
As regards the anatomic variations of the arteries,
a few of them were observed in our specimens. They
were related to a sporadic hypoplasia of some vessels
(the A1 segment and the P1 segment, as well as the
VA) in 1 case each, their “hyperplasia” (the PComA) in
1 case, early bifurcation (the M1 segment, and the SCA)
in one specimen each, and a single duplication (the SCA).
The AVMs pathogenesis
The AVMs consist of a group of abnormal tortuous
vessels (the nidus), the vascular core of which occurs
during the embryonic development in most cases
[16, 43, 53, 55, 78]. The majority of the arteries within
the AVMs undergo normal maturation in the prenatal
and postnatal period, but the veins retain some of
their embryonic features. The capillary network in
the nidus is either absent or contains some dilated
microvessels [16, 53, 55].
Due to the shunt of blood from the arteries directly
to the veins in many AVMs, a high blood flow appears,
663
which causes, among others, structural changes in
the vessel wall, and venous hypertension in the nidus
and the draining veins [4, 16, 24, 39, 43, 53, 55, 58].
This high venous pressure may lead to hypoperfusion
with resultant hypoxia or ischaemia in the local brain
parenchyma with consequent focal neurologic deficits
or epileptic focus formation [9, 29, 62, 80]. At the
same time, hypoxia and ischemia within the nidus
itself initiate an inflammatory response with produc-
tion of cytokines, which cause endothelium disorder
and activation of the angiogenic factors [47, 53]. The
resulting intranidal angiogenesis, along with the men-
tioned higher intranidal and postnidal venous pres-
sure, gradually remodel the AVMs vascular network.
Although AVMs incidence is very low in the gen-
eral population (0.02–0.05%) [32], they account for
up to 2% of all haemorrhagic strokes, thus markedly
contributing to the morbidity and mortality rate of
cerebrovascular disorders [8, 53, 58, 78, 80]. Be-
cause of that, any type of research in the AVMs field
is very important in understanding their structure,
pathophysiology, natural course, the angiographic
appearance, and neurologic consequences, as well
as in decisions regarding their therapy.
Anatomy of feeding arteries
As regards the identification of these vessels in
carotid and vertebral angiograms, our anatomic study
was of a great help, but also our previous experience in
the brain vasculature, as well as the angiographic data
reported by certain authors [7, 16, 46, 64, 68, 78].
As already mentioned, from 1 to 6 feeders were
seen to supply the corresponding AVMs in our study.
We counted, however, only the primary feeders, and
not their branches which entered the AVM. For ex-
ample, the frontopolar artery in Figure 3 divides into
two main branches which reached the AVM, but it
was classified as a singular feeding vessel.
The AVMs appeared more often in the supratento-
rial compartment (90.9%), and less frequently in the
infratentorial region (9.1%) of our patients (Table 1).
The latter frequency (9.1%) is within the range of
2–15% reported by other authors [5, 16, 24, 78]. The
parent vessel of the feeders was most often the MCA
in our patients, followed by the ACA and PCA, and less
frequently the ICA, AChA, PComA, BA and VA. Similar
results were reported by other authors [16, 78].
Obviously, the AVMs can be located in any part
of the brain, which means that any cerebral artery
can become a feeder [1, 5, 14, 16, 18, 24, 27, 33,
 Folia Morphol., 2018, Vol. 77, No. 4
34, 45, 46, 50, 51, 61, 65, 74, 78]. The type of the
feeding vessels depends firstly on a deep or superficial
AVMs position.
In the former case, the AVMs are mainly sup-
plied by the perforating vessels or the choroidal
arteries (Figs. 3, 10). These deep AVMs were rare
in our patients, as were in other reports which
mentioned a frequency of up to 18% [14, 24,
35, 70, 73]. As regards the type of the perfora-
tors, the latter authors identified the lenticulo-
striate arteries of the MCA, as well as the TPA of
the PCA, the perforators of the BA, and very rarely
the premammillary twig of the PComA (Fig. 10).
However, the thalamogeniculate vessels (Fig. 10)
have never been mentioned in literature as the AVMs
feeders. Nevertheless, these deep AVMs, either stri-
atal, thalamic, or those within the brain stem, are
most often manifested by focal neurologic deficits or
as an intracerebral or intraventricular haemorrhage.
Some perforating feeders could be damaged dur-
ing surgery of such AVMs [14, 45]. These feeders,
especially the lenticulostriate arteries and the perfora-
tors of the brain stem, must be preserved during the
intervention. Most often an endovascular treatment
or stereotactic radiosurgery are performed in these
patients, and less frequently a neurosurgical inter-
vention [14, 45, 70, 75, 79]. However, if radiologic
embolisation of a perforating feeder could cause seri-
ous local ischaemia, especially in the adjacent internal
capsule, in the thalamus, or within the important
brain stem structures, a microsurgical resection of
such an AVM is recommended [46].
The intraventricular, i.e. the thalamic AVMs in our
3 patients, received blood from the premammillary,
collicular, thalamoperforating, or thalamogeniculate
twigs, as well as from the corresponding choroidal
arteries, that is, the AChA, MPChA or LPChA (Fig. 10).
As for the TPA, one of them was reported to supply
a thalamic AVM from the opposite side [46]. Such
a perforator, which perfused both the right and left
thalamus, was observed in one of our anatomic spec-
imens. The other feeders mentioned in our patients
were noticed by certain authors as well [18, 26, 42,
61, 70], except the thalamogeniculate vessel and the
collicular artery. As regards the PICA’s choroidal twigs,
they are very rarely the feeders of the AVMs in the
region of the fourth ventricle [65, 74]. Nevertheless, in
patients with thalamic and intraventricular AVMs, the
radiologic endovascular treatment is usually applied
[18, 26, 51].
664
In the cases of superficial AVMs, which occur more
frequently than deeper ones, the leptomeningeal
(pial) vessels are most often engaged as the feeders.
As regards the ICA, a primitive trigeminal artery was
noticed in one of our patients, which supplied a small
perimesencephalic AVM. It was also rarely observed
by other authors to feed the cerebral AVMs of dif-
ferent locations [1, 44, 48]. The primitive trigeminal
artery may belong to various types. Namely, it may
connect the cavernous segment of the ICA with the
distal part of the BA, or may represent a cerebellar
artery (the SCA, AICA or PICA) arising from the ICA
instead of from the BA or the VA [1, 37, 48]. The
feeders originating from some other persistent em-
bryonal vessels were seen extremely rarely, e.g. from
the primitive olfactory or hypoglossal artery [28, 50].
Finally, some AVMs feeders are associated with the
arterial fenestration [71], and some others with the
moyamoya vessels [3, 49].
In our patients with the superficial AVMs, various
leptomeningeal branches were seen to be their feeders.
They commonly originated from the MCA, and less
frequently from the ACA, PCA, BA or VA (Tables 1, 2). In
general, our results are in accordance with other reports
[16, 24, 34, 50, 56, 61, 78]. Nevertheless, it is obvious
that the AVMs location and the position of the parent
arteries mainly determine the type of the feeders.
As regards the ACA in our patients, the medial orb-
itofrontal artery was not a feeder, nor the paracentral,
superior parietal, precuneal, and some internal frontal
arteries. In other reports, most often the pericallosal,
callosomarginal and frontopolar arteries of the ACA
were mentioned as the feeders, but not the internal
frontal, paracentral, and the superior parietal arteries
[16, 68, 78]. As regards the subcallosal branch of the
AComA, it was never seen to supply AVMs [16, 78].
In the MCA territory, the angular gyrus artery
was most often involved in our patients. The same
feeder was mentioned by certain authors [16, 61,
78], while the parietal vessels were reported by some
others [73]. On the other hand, the precentral and
temporal arteries were not observed as the feeders
in our patients, except the temporo-occipital artery.
Certain authors revealed some of them as the AVMs
supplying vessels, e.g. the anterior, middle, and pos-
terior temporal arteries [18].
The AChA contributed to a thalamic AVM supply in
only one of our patients. Other authors also noticed
this artery to perfuse some thalamic AVMsl, as well as
the choroidal and medial temporal ones [26, 42, 78].
 B. Milatović et al., Feeding arteries of the AVMs
In case of the AVMs in the PCA territory, the an-
terior and middle temporal arteries, as well as the
uncal, hippocampal and parahippocampal vessels,
were not the feeders in our patients. The AVMs was
most often supplied by the parieto-occipital artery,
and rarely by the calcarine and posterior temporal
vessels, as well as by the corresponding choroidal
arteries, i.e. the MPChA and the LPChA. The calcarine
feeder was infrequently mentioned in literature [33].
As regards the PComA, a contribution of its pre-
mammillary branch, found in one of our patients,
was very rarely reported by other authors [51, 61].
In the VA region, the perforating, anterolateral
and lateral medullary arteries, as well as the anterior
spinal artery, did not supply the AVMs in our patients,
but only the PICA in one case with multiple feeders
(Fig. 9). Some of the mentioned vessels were noticed
as the sporadic feeders in certain reports [24, 27].
As regards the BA, we found the cerebellar arteries,
i.e. the AICA and the SCA, to feed the AVMs, but not
the perforating, the anterolateral, inferolateral, super-
olateral, and posterolateral pontine twigs [15]. Certain
authors, however, identified some of these vessels as
supplying the AVMs of the brain stem in rare cases [24].
Finally, we observed some ECA branches in 3 pa-
tients (Table 1) to contribute to the leptomeningeal
AVMs supply, that is, the middle meningeal and the
occipital artery, respectively. Other authors found
sporadically the same arteries as the accessory AVMs
feeders [16, 41], and very rarely some of the persis-
tent primitive arteries in the dural region [28]. Some
authors registered dural vascular connections with
intraventricular AVMs [74]. According to certain re-
ports, some contribution of dural arteries is present
in more than 20% of patients, especially in those with
large superficial AVMs [31, 41].
There is a partial explanation of these events
from the anatomic aspect [11, 21]. Namely, some
cerebral arteries normally give rise to certain menin-
geal branches, e.g. the ICA (tentorial branch of the
meningohypophyseal trunk, and smaller branches
from the ophthalmic artery), the BA (some small
dural twigs), and the VA (the posterior meningeal
artery). Secondly, there are dural ECA branches as
well, e.g. the middle meningeal artery of the maxillary
artery, and small dural twigs of the occipital and the
ascending pharyngeal arteries. Some of these twigs
form the anastomotic channels among them in the
dural region where, in addition, sporadic pre-existing
small arteriovenous shunts are usually present. Such
665
vascular connections may develop into some larger
anastomotic and arteriovenous channels which can
form dural AVMs or dural arteriovenous fistulas [11,
16, 78]. In some way, certain dural vessels can become
the accessory feeders of some leptomeningeal AVMs,
or of combined dural and pial AVMs.
Clinical significance of the feeding arteries
Microcatheterisation of the feeders and their par-
ent arteries is a standard radiologic route to access
the AVMs and to perform their endovascular embo-
lisation [4, 16, 50–52, 68, 80]. It is understandable
that great care must be taken to avoid damage to the
feeders during such a procedure. Feeders’ anatomy is
important for microsurgical strategy as well [4, 14, 18,
24, 27, 45, 69, 75, 78, 80]. In some cases, certain lep-
tomeningeal feeding arteries, especially those of the
brainstem AVMs, can be surgically occluded with no
neurologic consequences [24, 27]. The crucial thing
is to perform occlusion close to the AVM, i.e. distal
to the intraparenchymal side branches of the feeders.
As regards the perforating feeders, these important
vessels must be spared during the intervention [45].
High blood flow velocity and the flow volume rate
in feeding arteries [4, 39, 43, 55, 58] can cause certain
structural changes in the vessel wall, that is, high-flow
angiopathy [8, 16, 55]. It may consist of splitting or
destruction of the internal elastic lamina, disorder of
the smooth muscle layer (hyperplasia, fibrosis of the
media coat, or focal disappearance of the smooth
muscle cells), as well as endothelial cells proliferation.
Some of these changes usually result in an en-
largement and tortuosity of the feeding arteries, as
seen in many of our patients, and as reported by
others [16, 68, 78]. Such feeders may occasionally
compress certain neural structures and thus cause
a neurologic manifestation, e.g. trigeminal neuralgia
[34]. The mentioned endothelial proliferation and
media coat changes can sometimes produce arterial
stenosis which, along with an additional process
of thrombosis or wall dissection, may progress to
a complete occlusion of a feeder [16, 23].
The mentioned high blood flow through the feed-
ers, along with decrease in or loss of vascular autoreg-
ulation, can result in a cerebral steal phenomenon.
The latter is manifested by a hypoperfusion of the
adjacent or distant regions of the brain with consec-
utive neurologic deficits [9, 16, 30, 59, 78]. However,
this mechanism has been debated for several decades
without a definite conclusion [16, 40].
 Folia Morphol., 2018, Vol. 77, No. 4
The mentioned haemodynamic processes in the
AVMs may have another consequence, that is, a cer-
tain endothelial disorder, activation of the coagu-
lation cascade and thrombosis of a feeding artery
[3, 23, 55]. An embolism of the feeders or their parent
arteries can occur as well, usually from the cardiac,
carotid, or aneurysmal sources. In this situation, two
consequences are possible. Firstly, a focal neurologic
deficit occurrence and, secondly, a spontaneous AVM
obliteration due to the intranidal stop of blood in
some cases [32]. In the former instance, a mechani-
cal endovascular thrombectomy of the parent artery
could be performed [2]. In the latter situation the pa-
tient is practically free from the AVM. Unfortunately,
such a spontaneous AVMs obliteration occurs in only
1–3% of patients [32].
In addition, a high blood flow within the feeders,
including a turbulence appearance and share stress
(i.e. the force which the blood exerts on the vessel
wall), can damage the vessel wall and thus cause an
aneurysm occurrence [1, 4, 8, 10, 16, 19, 54, 56, 77].
This is why the AVMs are relatively often associated
with cerebral aneurysms, either prenidal arterial, or
intranidal and postnidal venous aneurysms [10]. The
prenidal aneurysms, which belong to the saccular type,
are most often located on the feeding arteries, and
occasionally on their parent vessels. We noticed two
such aneurysms (2.6%), one of which was situated at
the branching site of the frontopolar artery (Fig. 2).
Certain radiologists mentioned the aneurysms frequen-
cy of 2.7–23.0% in patients with the AVMs [10, 16].
The presence of an aneurysm on a feeding artery
is very important clinically because it may rupture,
either spontaneously, or during or after an endovas-
cular radiologic procedure. In both cases, a dangerous
subarachnoid haemorrhage occurs or an intraparen-
chymal haematoma develops [10, 50, 54, 78]. As
regards the intranidal and postnidal venous pouches
and aneurysms, they are out of the scope of this study.
As already mentioned, the AVMs vasculature has
a certain risk of haemorrhage, which ranges between
0.9% to 34.3% of all the AVMs [8, 16, 36, 52, 58, 78].
The risk is higher in the AVMs with a single feeding
artery or with a single draining vein, in those with
combined deep and superficial drainage, or with an
infratentorial location, as well as in small-sized AVMs
with high blood pressure within the feeders, and in
the AVMs with coexisting aneurysms [36]. On the
other hand, the nonhaemorrhagic AVMs are usually
deeply located, with only perforating feeders, or with
666
more than three leptomeningeal feeders or three
draining veins [35].
In the cases of superficial (pial) AVMs bleeding,
the resulting subarachnoid haemorrhage causes occa-
sionally a vasospasm of the feeders [13, 78]. A spasm
may result in ischaemia of the brain parenchyma
and the appearance of certain neurologic symptoms
and signs. On the other hand, the spasm reduces
the AVMs flow, which can induce a spontaneous
thrombosis of the nidal vessels or draining veins in
some patients [32].
According to certain post-mortem investigations,
only 12% of the AVMs become symptomatic during
life [16]. As regards the clinical manifestations, a focal
motor or sensory deficit may occur, as well as dizzi-
ness, visual or speech disorders, or epileptic seizures
[9, 16, 23, 24, 29, 33, 35, 36, 62, 80]. Headaches are
one of the most frequent symptoms. Most often,
however, among the first signs of an AVM presence
is intracranial bleeding, either in the form of intracer-
ebral hematoma, or subarachnoid or intraventricular
haemorrhage [8, 16, 36, 52, 58, 78]. In our group,
haemorrhage was the first sign of an AVM in 63.6% of
patients, which is within a range of 30–82% reported
by other authors [16].
The AVMs diagnosis is commonly made by a CT or
magnetic resonance imaging (MRI) examination, but
the most precise data can be obtained by performing
a standard digital subtraction angiography [7, 16, 68].
In addition, 3D angiography is also used occasionally,
as well as its combination with MRI scans, that is, the
image fusion method [60, 62, 63].
Finally, there are three main therapeutic tech-
niques in the AVMs patients: a direct microsurgical
resection, endovascular radiologic embolisation, and
stereotactic radiosurgery, including their combina-
tions sporadically [16, 24, 52, 60, 68–70, 78, 79]. In
our patients, each of these techniques was used, ei-
ther as a single method or in combination with other
interventions. According to our study and the men-
tioned reports, deep AVMs should be predominantly
treated by endovascular embolisation or radiosurgery,
whilst the leptomeningeal ones by embolisation and,
when necessary, by surgery. According to some au-
thors, the success of such treatments is about 92%
[80]. Our patients showed a similar outcome (89.6%).
CONCLUSIONS
Arteriovenous malformations are very important
disorders in human cerebrovascular pathology. They
 B. Milatović et al., Feeding arteries of the AVMs
are fed by various branches of the main cerebral
arteries, that is, the perforating, choroidal or, most
often, leptomeningeal. One or more of the feed-
ers most frequently arise from the middle, anterior,
and posterior cerebral arteries, and rarely from the
infratentorial vessels. Knowledge of the anatomic
features of the feeding arteries is very important in
diagnostics, therapy and prognosis of AVMs.
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